ABSTRACT

Context Sugar-sweetened beverages like soft drinks and fruit punches contain
large amounts of readily absorbable sugars and may contribute to weight gain
and an increased risk of type 2 diabetes, but these relationships have been
minimally addressed in adults.

Objective To examine the association between consumption of sugar-sweetened beverages
and weight change and risk of type 2 diabetes in women.

Design, Setting, and Participants Prospective cohort analyses conducted from 1991 to 1999 among women
in the Nurses' Health Study II. The diabetes analysis included 91 249
women free of diabetes and other major chronic diseases at baseline in 1991.
The weight change analysis included 51 603 women for whom complete dietary
information and body weight were ascertained in 1991, 1995, and 1999. We identified
741 incident cases of confirmed type 2 diabetes during 716 300 person-years
of follow-up.

Main Outcome Measures Weight gain and incidence of type 2 diabetes.

Results Those with stable consumption patterns had no difference in weight gain,
but weight gain over a 4-year period was highest among women who increased
their sugar-sweetened soft drink consumption from 1 or fewer drinks per week
to 1 or more drinks per day (multivariate-adjusted means, 4.69 kg for 1991
to 1995 and 4.20 kg for 1995 to 1999) and was smallest among women who decreased
their intake (1.34 and 0.15 kg for the 2 periods, respectively) after adjusting
for lifestyle and dietary confounders. Increased consumption of fruit punch
was also associated with greater weight gain compared with decreased consumption.
After adjustment for potential confounders, women consuming 1 or more sugar-sweetened
soft drinks per day had a relative risk [RR] of type 2 diabetes of 1.83 (95%
confidence interval [CI], 1.42-2.36; P<.001 for
trend) compared with those who consumed less than 1 of these beverages per
month. Similarly, consumption of fruit punch was associated with increased
diabetes risk (RR for ≥1 drink per day compared with <1 drink per month,
2.00; 95% CI, 1.33-3.03; P = .001).

Conclusion Higher consumption of sugar-sweetened beverages is associated with a
greater magnitude of weight gain and an increased risk for development of
type 2 diabetes in women, possibly by providing excessive calories and large
amounts of rapidly absorbable sugars.

Figures in this Article

Type 2 diabetes mellitus affects about 17 million US individuals.1- 3 The prevalence of diabetes
has increased rapidly during the last decades2,4,5 in
parallel to the obesity epidemic.2,5 Coinciding
with the increasing prevalence of obesity and type 2 diabetes, soft drink
consumption in the United States increased by 61% in adults from 1977 to 19976 and more than doubled in children and adolescents
from 1977-1978 to 1994-1998.7 Recent evidence
suggests an association between the intake of sugar-sweetened soft drinks
and the risk of obesity in children,8 but data
among adults are limited. Besides contributing to obesity, sugar-sweetened
soft drinks might increase risk of diabetes because they contain large amounts
of high-fructose corn syrup, which raises blood glucose similarly to sucrose.9 Soft drinks are the leading source of added sugars
in the US diet,10 and each serving represents
a considerable amount of glycemic load that may increase risk of diabetes.11 In addition, cola-based soft drinks contain caramel
coloring, which is rich in advanced glycation end products that might increase
insulin resistance12 and inflammation.13 However, no study has examined the association between
the consumption of soft drinks and other sugar-sweetened beverages and risk
of type 2 diabetes. We therefore examined the relationships between sugar-sweetened
beverage consumption and weight gain and diabetes risk in a large cohort of
young and middle-aged women, controlling for potential confounding factors.
Because the majority of sugar-sweetened beverages consumed in this cohort
are soft drinks, we particularly emphasized soft drink consumption.

METHODS

Study Population

The Nurses' Health Study II is a prospective cohort study of 116 671
female US nurses aged 24 to 44 years at study initiation in 1989. This cohort
is followed up using biennial mailed questionnaires, with a follow-up rate
exceeding 90% for every 2-year period. For the analyses presented here, women
were excluded if they did not complete a dietary questionnaire in 1991 or
if more than 9 items on it were left blank; if the reported dietary intake
was implausible with regard to total energy intake (ie, <500 kcal/d or
>3500 kcal/d); if they had a history of diabetes, cancer (except nonmelanoma
skin cancer), or cardiovascular disease at baseline; or if they had not provided
data on physical activity in 1991. The final sample for the diabetes analysis
consisted of 91 249 women. For the analysis on weight change, we also
excluded women who did not complete questions on sugar-sweetened soft drink
consumption, who had a history of diabetes or cardiovascular disease before
1995 or reported the diagnosis of cancer (except nonmelanoma skin cancer)
on any questionnaire, who did not report body weight on any questionnaire,
or who had no data on physical activity assessed in 1997. These exclusions
left a total of 51 603 women for the analyses. The study was approved
by the human research committees at the Harvard School of Public Health and
Brigham and Women's Hospital, Boston, Mass; completion of the self-administered
questionnaire was considered to imply informed consent.

Dietary Assessment

In 1991, the mailed questionnaire included a 133-item semiquantitative
food frequency questionnaire. Women were asked how often they had consumed
a commonly used unit or portion size of each food on average over the previous
year, including 3 items on consumption of sugar-sweetened soft drinks ("Coke,
Pepsi, or other cola with sugar," "caffeine-free Coke, Pepsi, or other cola
with sugar," and "other carbonated beverages with sugar"), 4 items on fruit
juice ("apple juice," "orange juice," "grapefruit juice," and "other juice"),
1 item on fruit punch, and 3 items on diet soft drinks ("low-calorie cola
with caffeine," "low-calorie caffeine-free cola," and "other low-calorie beverages").
We summed the intake of single items to create a total of sugar-sweetened
soft drink, diet soft drink, and fruit juice consumption. The 9 possible responses,
ranging from "never" to "6 or more times per day," were aggregated into 4
categories (<1 drink per month, 1-4 drinks per month, 2-6 drinks per week,
and ≥1 drink per day). Similar questionnaires were used to collect dietary
information in 1995 and 1999. Nutrient intakes were computed by multiplying
the frequency response by the nutrient content of the specified portion sizes.
Values for nutrients were derived from the US Department of Agriculture sources14 and supplemented with information from manufacturers.
The validity and reliability of food frequency questionnaires similar to those
used in the Nurses' Health Study II have been described elsewhere.15,16 Briefly, the correlation coefficients
between questionnaire and multiple dietary records were 0.84 for cola-type
soft drinks (sugar-sweetened and diet combined), 0.36 for other carbonated
soft drinks, 0.84 for orange juice, and 0.56 for fruit punch in the Nurses'
Health Study I15 and were 0.84 for sugar-sweetened
cola, 0.55 for other sugar-sweetened soft drinks, 0.73 for diet cola, 0.74
for other diet soft drinks, 0.78 for orange juice, 0.77 for apple juice, 0.75
for grapefruit juice, and 0.89 for other fruit juices in the Health Professionals
Follow-up Study,16 2 similar cohort studies
among US health care professionals.

Assessment of Nondietary Exposures

Information on age, weight, smoking status, contraceptive use, postmenopausal
hormone therapy, and pregnancies was collected on biennial questionnaires.
We calculated body mass index (BMI) as weight in kilograms divided by the
square of height in meters; height was assessed at baseline only. Self-reports
of body weight were highly correlated with technician-measured weights (r = 0.96) in the Nurses' Health Study I.17 Family
history of diabetes was reported in 1989 only. In 1991 and 1997, participants
were asked how many flights of stairs they climb daily and the amount of time
per week they spent on average on each of the following activities: walking
or hiking outdoors; jogging; running; bicycling; lap swimming; tennis, squash,
or racquetball playing; calisthenics; and other aerobic recreation. From this
information, weekly energy expenditure in metabolic equivalent hours was calculated,
weighting each activity by its intensity level.18 Physical
activity reported on the questionnaire was highly correlated with activity
recorded in diaries or by 24-hour recall (0.79 vs 0.62).19 Because
physical activity was not assessed in 1995 or 1999, for our analysis on weight
change, we used the 1997 estimate for both of these time points instead.

Ascertainment of Type 2 Diabetes

Women reporting a new diagnosis of diabetes on any of the biennial questionnaires
were sent supplementary questionnaires asking about diagnosis and treatment
of their diabetes, as well as history of ketoacidosis to confirm the self-report
and to distinguish between type 1 and type 2 diabetes. In accordance with
the criteria of the National Diabetes Data Group,20 confirmation
of diabetes required at least 1 of the following: (1) an elevated plasma glucose
concentration (fasting plasma glucose ≥7.8 mmol/L [140 mg/dL], random plasma
glucose ≥11.1 mmol/L [200 mg/dL], and/or plasma glucose ≥11.1 mmol/L
[200 mg/dL] after ≥2 hours during an oral glucose tolerance test) plus
at least 1 classic symptom (excessive thirst, polyuria, weight loss, or hunger);
(2) no symptoms but at least 2 elevated plasma glucose concentrations (by
the aforementioned criteria) on different occasions; or (3) treatment with
hypoglycemic medication (insulin or oral hypoglycemic agent). We used the
National Diabetes Data Group criteria to define diabetes because the majority
of our cases were diagnosed prior to the release of the American Diabetes
Association criteria in 1997.21 In substudies
of the Nurses' Health Study I and the Health Professionals Follow-up Study,
98% and 97% of the self-reported diabetes cases documented by the same supplementary
questionnaire were confirmed by medical record review.22,23

Statistical Analysis

We calculated the mean weight changes for groups defined by change in
soft drink consumption from 1991 to 1995 and from 1995 to 1999, adjusting
for age, alcohol intake, physical activity, smoking, BMI, and other lifestyle
and dietary confounders at baseline for each period. We also adjusted for
food items that have been previously shown to be associated with sugar-sweetened
soft drink consumption.24 We additionally adjusted
for changes in these covariates (except BMI) during the period 1991 to 1995
in a separate model for that period.

We estimated the relative risk (RR) of diabetes for each category of
intake compared with the lowest category using Cox proportional hazards analysis
stratified by 5-year age categories and 2-year intervals. Duration of follow-up
was calculated as the interval between the return of the 1991 questionnaire
and diagnosis of diabetes, death, or June 1, 1999. The 1991 intake was used
for the follow-up between 1991 and 1995, and the average of the 1991 and 1995
intakes was used for the follow-up between 1995 and 1999 to reduce within-participant
variation and to best represent long-term diet.25 We
used the 1991 but not the 1995 intake data for individuals who reported on
the 1993 or 1995 questionnaire a diagnosis of cancer (except nonmelanoma skin
cancer) or cardiovascular disease because changes in diet after development
of these conditions may confound the relationship between dietary intake and
diabetes.25

We used information on covariates obtained from the baseline or subsequent
questionnaires in multivariate analyses. Because BMI and total energy intake
might represent intermediate end points or pathways rather than confounders
for sugar-sweetened soft drinks, we adjusted for BMI and total caloric intake
in separate models. Nondietary covariates were updated during follow-up using
the most recent data for each 2-year follow-up interval. The significance
of linear trends across categories of beverage consumption was tested by assigning
to each participant the median value for the category and modeling this value
as a continuous variable. We evaluated whether the association between sugar-sweetened
soft drink consumption and risk of diabetes was modified by BMI, physical
activity, and a family history of diabetes using analyses stratified by these
variables and by modeling interaction terms.

All P values presented are 2-tailed; P<.05 was considered statistically significant. All
statistical analyses were performed using SAS software, version 8.0 (SAS Institute
Inc, Cary, NC).

RESULTS

Sugar-Sweetened Beverages and Weight Change

Women with a higher intake of sugar-sweetened soft drinks tended to
be less physically active, to smoke more, and to have higher intake of total
energy and lower intake of protein, alcohol, magnesium, and cereal fiber (Table 1). Intake of total carbohydrates,
sucrose, and fructose as well as the overall glycemic index were higher in
women with greater sugar-sweetened soft drink consumption, but starch intake
was lower.

Women who increased their sugar-sweetened soft drink consumption between
1991 and 1995 from low (≤1/wk) to high (≥1/d) (n = 1007) also increased
their reported total energy intake by 358 kcal/d on average (Figure 1). In contrast, women who reduced their sugar-sweetened
soft drink consumption between 1991 and 1995 (n = 1020) also reduced their
total energy consumption by 319 kcal/d on average. Changes in energy intake
from food sources other than sugar-sweetened soft drinks accounted for only
27% to 34% of these changes in total energy intake. Similar associations were
observed for the period 1995-1999.

Figure 1. Mean Change in Energy Consumption
According to Time Trends in Sugar-Sweetened Soft Drink Consumption Between
1991 and 1995 in 51 603 Women

For both periods 1991 to 1995 and 1995 to 1999, women who increased
their consumption of sugar-sweetened soft drinks from low to high had significantly
larger increases in weight (multivariate-adjusted means, 4.69 kg during 1991-1995
and 4.20 kg during 1995-1999) and BMI (multivariate-adjusted means, 1.72 during
1991-1995 and 1.53 during 1995-1999) than women who maintained a low or a
high intake or substantially reduced their intake (P<.001)
(Table 2). The lowest weight gain
and increase in BMI were observed among women who reduced their intake from
high to low (multivariate-adjusted mean change in weight, 1.34 kg during 1991-1995
and 0.15 kg during 1995-1999; respective multivariate-adjusted mean change
in BMI, 0.49 and 0.05). Because lifestyle and dietary changes might confound
these associations, we repeated the analysis for the period 1991 to 1995,
additionally controlling for changes in physical activity and other covariates
over time, but results remained similar. We repeated our analysis excluding
all women who reported a pregnancy in 1991, 1995, or 1999, but this had minimal
impact on our observations (data not shown).

Women who increased consumption of fruit punch from 1 drink or less
per week in 1991 to 1 drink or more per day in 1995 gained more weight (3.69
kg) compared with women who decreased consumption (2.43 kg; P<.001). Similarly, increased consumption of fruit juice was associated
with larger weight gain (4.03 kg) compared with decreased fruit juice consumption
(2.32 kg) (P<.001). In contrast with sugar-sweetened
beverages, weight gain in participants who increased their diet soft drink
consumption from 1 drink or less per week in 1991 to 1 drink or more per day
in 1995 (1.59 kg) was significantly lower compared with women who decreased
their diet soft drink consumption from 1 drink or more per day in 1991 to
1 drink or less per week in 1995 (4.25 kg) (P<.001).

Women who increased their soft drink consumption from 1991 to 1995 and
maintained a high level of intake during 1995-1999 gained, on average, 8.0
kg between 1991 and 1999, whereas women who decreased their consumption between
1991 and 1995 and maintained a low level of intake gained 2.8 kg between 1991
and 1999 on average (Figure 2).

Figure 2. Mean Weight in 1991, 1995, and 1999
According to Trends in Sugar-Sweetened Soft Drink Consumption in 1969 Women
Who Changed Consumption From 1991 to 1995 and Either Changed or Maintained
Level of Consumption Until 1999

Low and high intakes were defined as 1 drink or less per week and
1 drink or more per day, respectively. The number of participants were: low-high-high,
323; low-high-low, 461; high-low-high, 110; and high-low-low, 746. Groups
with similar intake in 1991 and 1995 were combined for estimates for these
time points. Means were adjusted for age, alcohol intake, physical activity,
smoking, postmenopausal hormone use, oral contraceptive use, cereal fiber
intake, and total fat intake at each time point. P =
.02 for difference between low-high-high intake and low-high-low intake and
for difference between high-low-high intake and high-low-low intake.

Sugar-Sweetened Beverages and Risk of Diabetes

During 716 300 person-years of follow-up, we documented 741 new
cases of type 2 diabetes. Greater sugar-sweetened soft drink consumption was
strongly associated with progressively higher risk of type 2 diabetes (Table 3). The age-adjusted RR was 1.98
(95% confidence interval [CI], 1.60-2.44) for women consuming 1 or more sugar-sweetened
soft drinks per day compared with those consuming less than 1 sugar-sweetened
soft drink per month. This association was slightly attenuated after adjustment
for lifestyle and dietary confounders (RR for extreme categories, 1.83; 95%
CI, 1.42-2.36; P<.001 for trend). The RR for extreme
categories further controlling for BMI was 1.39 (95% CI, 1.07-1.76; P = .01 for trend). This finding suggests that BMI accounted
for about half of the excess risk. Adjustment for caloric intake in addition
to BMI further attenuated the association, but sugar-sweetened soft drinks
remained significantly associated with an increased risk of diabetes (RR for
extreme categories, 1.32; 95% CI, 1.01-1.73; P =
.04 for trend). The results for sugar-sweetened cola alone were similar to
those for all sugar-sweetened soft drinks (Table 3). Similar to sugar-sweetened soft drinks, fruit punch consumption
was significantly associated with diabetes risk. The multivariate RR for fruit
punch consumption of 1 drink or more per day compared with less than 1 drink
per month was 2.00 (95% CI, 1.33-3.03; P = .001 for
trend).

Diet soft drink consumption was associated with a slight, nonsignificant
increased diabetes risk after additional adjustment for baseline BMI. The
RR for diet soft drink consumption of 1 or more drinks per day compared with
less than 1 drink per month was 1.21 (95% CI, 0.97-1.50; P = .12 for trend). Relative risk remained unchanged after additional
adjustment for caloric intake.

Fruit juice consumption was not associated with diabetes risk. The multivariate-adjusted
RR of diabetes comparing women who consumed more than 1 drink per day of fruit
juices with women who consumed less than 1 drink per month of fruit juices
was 0.97 (95% CI, 0.64-1.47; P = .84 for trend).

COMMENT

In this 8-year follow-up study of women, we found positive associations
between sugar-sweetened beverage consumption and both greater weight gain
and risk of type 2 diabetes, independent of known risk factors.

Sugar-sweetened soft drinks may contribute to weight gain because of
the low satiety of liquid foods. Energy provided by sugar-sweetened beverages
does not affect subsequent food and energy intake in short-term human studies.26- 28 Similarly, in experimental
animals, intake of sugar-sweetened beverages is not fully compensated by reductions
in intake of solid foods, resulting in a positive caloric balance and development
of obesity.29 Consequently, consumption of
sugar-sweetened soft drinks significantly increased caloric intake and body
weight over a 3-week period in normal-weight adults,30 and
supplementing sucrose, mainly in the form of sugar-sweetened soft drinks,
over a 10-week period to ad libitum diets in overweight men and women resulted
in an increase in energy intake and body weight (by 1.6 kg) compared with
decreases with artificially sweetened supplements (by 0.3 kg).31 Consumption
of sugar-sweetened soft drinks has also been associated with greater risk
of obesity in children,8 while consumption
of diet soft drinks has not. Interestingly, in our study, women who increased
their sugar-sweetened soft drink consumption also increased energy intake
from other foods, indicating that these beverages may even induce hunger and
food intake. However, experimental data on soft drink consumption and food
intake have not provided support for this hypothesis.32,33 Our
observation may, therefore, rather reflect dietary and lifestyle changes accompanying
changes in soft drink consumption.

We observed no difference in weight change between women with consistently
low or high sugar-sweetened soft drink consumption. The lower weight gain
associated with reduction of sugar-sweetened soft drink consumption compared
with stable intake suggests that women do benefit from decreasing consumption
but that weight trajectories do not continue to diverge with time. Long-term
effects of sugar-sweetened beverages on body weight have not been studied
in experimental settings so far, and further research is warranted.

Besides their potential contribution to weight gain, sugar-sweetened
soft drinks might also increase risk of type 2 diabetes because of their high
amount of rapidly absorbable carbohydrates. They contain large amounts of
high-fructose corn syrup, which has similar effects on blood glucose as sucrose,9 and consumption of sugar-sweetened soft drinks induces
a fast and dramatic increase in both glucose and insulin concentrations.34 Sugar-sweetened soft drinks therefore contribute
to a high glycemic index of the overall diet, a risk factor for diabetes in
this study population35 and other cohort studies.11 In addition, cola-type soft drinks contain caramel
coloring, which is rich in advanced glycation end products, which may increase
insulin resistance12 and inflammation.13 However, diet cola was generally not associated with
diabetes risk after adjustment for BMI. Advanced glycation end products therefore
appear unlikely to account for the association between sugar-sweetened soft
drinks and diabetes. In addition, soft drinks often contain caffeine, which
might reduce diabetes risk.36,37 However,
the caffeine content of soft drinks (10-16 mg per 100 g) is considerably less
than in coffee (35-75 mg per 100 g) or black tea (about 22 mg per 100 g) and
soft drinks might therefore contribute moderately to variation in total caffeine
consumption in the adult US population. In our study population, adjustment
for caffeine did not alter the association for soft drinks.

Fruit juice consumption was not associated with diabetes risk in our
study, which suggests that naturally occurring sugars in beverages may have
different metabolic effects than added sugars. Fruit juices generally have
a lower glycemic index than sugar-sweetened soft drinks and fruit punches.38 In addition, vitamins, minerals, soluble fiber, and
phytochemicals in fruit juices may have beneficial effects counterbalancing
potential adverse effects of sugars. In contrast, fruit punches contain only
a small proportion of fruit juice but large amounts of added high-fructose
corn syrup and, therefore, provide little nutritional value compared with
pure fruit juices. Our finding that fruit punch consumption was associated
with increased diabetes risk suggests that its physiological consequences
may be similar to sugar-sweetened soft drinks.

Imprecise dietary measurement could potentially have influenced our
observed associations. However, random errors in dietary assessment measures
might have accounted for a lack of association but not the reverse.25 The repeated dietary measurements made in this study
were an advantage because they reduce measurement errors and account for changes
in eating patterns over time.25 Because of
the observational nature of the study, we cannot prove that the observed associations
are causal because residual confounding could theoretically affect the observed
associations. However, we controlled for potential confounding by most known
risk factors that are plausibly associated with soft drink consumption and
changes in these variables over time. Consistent with our observation, supplementation
of sucrose, mainly in the form of soft drinks, resulted in increased energy
consumption in an experimental study, with the increase largely attributable
to the increased sucrose intake.31 A further
limitation of our study is the reliance on self-reported body weight. It is
possible that underreporting of body weight, particularly among heavier women,
may have led to an underestimation of weight gain. However, correlation between
self-reported and technician-measured body weight was found to be high in
a similar cohort of older female nurses,17 and
underreporting may be less prevalent among relatively young women.39 Also, we used the National Diabetes Data Group criteria
to define diabetes,20 but the diagnostic criteria
were changed in 199721 such that lower fasting
glucose levels would be considered diagnostic. The majority of our cases were
diagnosed prior to the release of the revised criteria in 1997; the incidence
of diabetes in our cohort is therefore likely an underestimation.

In conclusion, our findings suggest that frequent consumption of sugar-sweetened
beverages may be associated with larger weight gain and increased risk of
type 2 diabetes, possibly by providing excessive calories and large amounts
of rapidly absorbable sugars. Public health strategies to prevent obesity
and type 2 diabetes should focus on reducing sugar-sweetened beverage consumption.

REFERENCES

Centers for Disease Control and Prevention. National Diabetes Fact Sheet: General Information
and National Estimates on Diabetes in the United States, 2000.Atlanta, Ga: Centers for Disease Control and Prevention; 2002.

Figure 1. Mean Change in Energy Consumption
According to Time Trends in Sugar-Sweetened Soft Drink Consumption Between
1991 and 1995 in 51 603 Women

Figure 2. Mean Weight in 1991, 1995, and 1999
According to Trends in Sugar-Sweetened Soft Drink Consumption in 1969 Women
Who Changed Consumption From 1991 to 1995 and Either Changed or Maintained
Level of Consumption Until 1999

Low and high intakes were defined as 1 drink or less per week and
1 drink or more per day, respectively. The number of participants were: low-high-high,
323; low-high-low, 461; high-low-high, 110; and high-low-low, 746. Groups
with similar intake in 1991 and 1995 were combined for estimates for these
time points. Means were adjusted for age, alcohol intake, physical activity,
smoking, postmenopausal hormone use, oral contraceptive use, cereal fiber
intake, and total fat intake at each time point. P =
.02 for difference between low-high-high intake and low-high-low intake and
for difference between high-low-high intake and high-low-low intake.

References

Centers for Disease Control and Prevention. National Diabetes Fact Sheet: General Information
and National Estimates on Diabetes in the United States, 2000.Atlanta, Ga: Centers for Disease Control and Prevention; 2002.

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